The evolutionary history and mechanistic basis of female ornamentation in a tropical songbird

Abstract

Ornamentation, such as the showy plumage of birds, is widespread among female vertebrates, yet the evolutionary pressures shaping female ornamentation remain uncertain. In part this is due to a poor understanding of the mechanistic route to ornamentation in females. To address this issue, we evaluated the evolutionary history of ornament expression in a tropical passerine bird, the White-shouldered Fairywren, whose females, but not males, strongly vary between populations in occurrence of ornamented black-and-white plumage. We first use phylogenomic analysis to demonstrate that female ornamentation is derived and that female ornamentation evolves independently of changes in male plumage. We then use exogenous testosterone in a field experiment to induce partial ornamentation in naturally unornamented females. By sequencing the transcriptome of experimentally induced ornamented and natural feathers, we identify genes expressed during ornament production and evaluate the degree to which female ornamentation in this system is associated with elevated testosterone, as is common in males. We reveal that some ornamentation in females is linked to testosterone and that sexes differ in ornament-linked gene expression. Lastly, using genomic outlier analysis we identify a candidate melanogenesis gene that lies in a region of high genomic divergence among populations that is also differentially expressed in feather follicles of different female plumages. Taken together, these findings are consistent with sex-specific selection favoring the evolution of female ornaments and demonstrate a key role for testosterone in generating population divergence in female ornamentation through gene regulation. More broadly, our work highlights similarities and differences in how ornamentation evolves in the sexes.

The evolution of sex similarities in social signals: Climatic seasonality is associated with lower sexual dimorphism and greater elaboration of female and male signals in antbirds (Thamnophilidae)

“…2000), whereas plumage coloration is a short distance signal (Uy and Safran 2013) that may mediate aggressive territorial interactions similarly in both sexes (Enbody et al. 2018, 2022; Macedo et al. 2021).…”

“…Taxa with low sexual dimorphism may indicate that both sexes engage in social competition with similar intensities and not that social selection is weaker (Enbody et al. 2018, 2022; Beco et al. 2021; Macedo et al.…”

“…In contrast to visual signals, we did not observe effects of climatic seasonality on sexual dimorphism of acoustic signals, suggesting that factors affecting sexual dimorphism differ between these signal modalities. For instance, sexually dimorphic songs may facilitate sex identification in long-distance mate attraction in densely vegetated habitats (Morton et al 2000), whereas plumage coloration is a short distance signal (Uy and Safran 2013) that may mediate aggressive territorial interactions similarly in both sexes (Enbody et al 2018(Enbody et al , 2022Macedo et al 2021). However, even in visual signals, there was great variation in the degree of sexual dichromatism across climatic gradients.…”

“…Our study suggests that, across diverse taxa and environments, female signals as well as male signals may respond to seasonally varying resources depending on how each sex is affected by natural and social selection. Taxa with low sexual dimorphism may indicate that both sexes engage in social competition with similar intensities and not that social selection is weaker (Enbody et al 2018(Enbody et al , 2022Beco et al 2021;Macedo et al 2021;Odom et al 2021).…”

Unexpected long-term retention of subcutaneous beeswax implants and additional notes on dose and composition from four testosterone implant studies

“…For several decades subcutaneous testosterone implants using silastic tubing have been used in wild animals to determine which traits are sensitive to enhanced testosterone circulation (Balthazart et al, 1983;Boersma et al, 2020;Cordero, 2008;Enbody et al, 2022;Fusani, 2008;Lahaye et al, 2014;Lindsay et al, 2016Lindsay et al, , 2011Muck and Goymann, 2018;Sandell, 2007). Yet, two challenges of testosterone implants endure today: 1) ensuring the dose is physiologically relevant, and 2) designing minimally invasive implants that do not require recapture and removal.…”